Full sequence and comparative analysis of the plasmid pAPEC-1 of avian pathogenic E. coli χ7122 (O78:k80:H9)

PLoS ONE

Volumn 4, Issue 1, 2009, Pages

  Mellata, Melha ^a   Touchman, Jeffrey W ^b   Curtis III, Roy ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLICIN; COLICIN V; ESCHERICHIA COLI PROTEIN; HEMAGGLUTININ; PROTEIN ETSABC; PROTEIN HLYF; PROTEIN HOK; PROTEIN IROBCDN; PROTEIN ISS; PROTEIN IUCABCD; PROTEIN IUTA; PROTEIN OMPT; PROTEIN REPFIB; PROTEIN REPFIC; PROTEIN REPFIIA; PROTEIN SITABCD; PROTEIN SOK; PROTEIN SRNB; PROTEIN TRA; PROTEIN TSH; UNCLASSIFIED DRUG; PRIMER DNA;

ARTICLE; AVIAN PATHOGENIC ESCHERICHIA COLI; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BLOOD GROUP TYPING; CONTROLLED STUDY; ENTEROBACTERIACEAE INFECTION; GENE FUNCTION; GENE IDENTIFICATION; GENE INSERTION SEQUENCE; GENE REARRANGEMENT; GENE SEGREGATION; GENE TRANSFER; GENETIC ASSOCIATION; GENETIC VARIABILITY; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PLASMID; POLYMERASE CHAIN REACTION; REPLICON; SEQUENCE ANALYSIS; TEMPERATURE SENSITIVITY; ANIMAL; BACTERIAL GENOME; BIOLOGICAL MODEL; CHEMISTRY; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENETICS; GENOME; GENOMICS; HORIZONTAL GENE TRANSFER; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; VIRULENCE;

ANIMALIA; AVES;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENE TRANSFER, HORIZONTAL; GENOME; GENOME, BACTERIAL; GENOMICS; HUMANS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; VIRULENCE;

EID: 58849136299     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004232     Document Type: Article

References (84)

1. Ziebuhr W, Ohlsen K, Karch H, Korhonen T, Hacker J (1999) Evolution of bacterial pathogenesis. Cell Mol Life Sci 56: 719-728.
2. Barnes HJ, J. V, Gross. WB (2003) Colibacillosis. In: Saif SY, ed. Diseases of poultry. Ames, Iowa: Iowa State University Press. pp 631-652.
3. Dho-Moulin M, Fairbrother JM (1999) Avian pathogenic Escherichia coli (APEC). Vet Res 30: 299-316.
4. Ewers C, Li G, Wilking H, Kiessling S, Alt K, et al. (2007) Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int J Med Microbiol 297: 163-176.
5. Moulin-Schouleur M, Reperant M, Laurent S, Bree A, Mignon-Grasteau S, et al. (2007) Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 45: 3366-3376.
6. Russo TA, Johnson JR (2000) Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 181: 1753-1754.
7. Dozois CM, Daigle F, Curtiss III R (2003) Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc Natl Acad Sci U S A 100: 247-252.
8. Johnson TJ, Giddings CW, Horne SM, Gibbs PS, Wooley RE, et al. (2002) Location of increased serum survival gene and selected virulence traits on a conjugative R plasmid in an avian Escherichia coli isolate. Avian Dis 46: 342-352.
9. Stehling EG, Yano T, Brocchi M, da Silveira WD (2003) Characterization of a plasmid-encoded adhesin of an avian pathogenic Escherichia coli (APEC) strain isolated from a case of swollen head syndrome (SHS). Vet Microbiol 95: 111-120.
10. Johnson TJ, Skyberg J, Nolan LK (2004) Multiple antimicrobial resistance region of a putative virulence plasmid from an Escherichia coli isolate incriminated in avian colibacillosis. Avian Dis 48: 351-360.
11. Tivendale KA, Allen JL, Ginns CA, Crabb BS, Browning GF (2004) Association of iss and iucA, but not tsh, with plasmid-mediated virulence of avian pathogenic Escherichia coli. Infect Immun 72: 6554-6560.
12. Skyberg JA, Johnson TJ, Johnson JR, Clabots C, Logue CM, et al. (2006) Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine, and colonize the murine kidney. Infect Immun 74: 6287-6292.
13. Smith HW, Huggins MB (1980) The association of the O18, K1 and H7 antigens and the ColV plasmid of a strain of Escherichia coli with its virulence and immunogenicity. J Gen Microbiol 121: 387-400.
14. Wooley RE, Gibbs PS, Brown TP, Glisson JR, Steffens WL, et al. (1998) Colonization of the chicken trachea by an avirulent avian Escherichia coli transformed with plasmid pHK11. Avian Dis 42: 194-198.
15. Johnson TJ, Siek KE, Johnson SJ, Nolan LK (2006) DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol 188: 745-758.
16. Dozois CM, Dho-Moulin M, Bree A, Fairbrother JM, Desautels C, et al. (2000) Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the Tsh genetic region. Infect Immun 68: 4145-4154.
17. Doetkott DM, Nolan LK, Giddings CW, Berryhill DL (1996) Large plasmids of avian Escherichia coli isolates. Avian Dis 40: 927-930.
18. Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK (2005) Characterizing the APEC pathotype. Vet Res 36: 241-256.
19. Johnson TJ, Johnson SJ, Nolan LK (2006) Complete DNA sequence of a ColBM plasmid from avian pathogenic Escherichia coli suggests that it evolved from closely related ColV virulence plasmids. J Bacteriol 188: 5975-5983.
20. Mellata M, Dho-Moulin M, Dozois CM, Curtiss III R, Lehoux B, et al. (2003) Role of avian pathogenic Escherichia coli virulence factors in bacterial interaction with chicken heterophils and macrophages. Infect Immun 71: 494-503.
21. Mellata M, Dho-Moulin M, Dozois CM, Curtiss III R, Brown PK, et al. (2003) Role of virulence factors in resistance of avian pathogenic Escherichia coli to serum and in pathogenicity. Infect Immun 71: 536-540.
22. Brown PK, Curtiss III R (1996) Unique chromosomal regions associated with virulence of an avian pathogenic Escherichia coli strain. Proc Natl Acad Sci U S A 93: 11149-11154.
23. Ozanne G, Mathieu LG, Baril JP (1977) Production of colicin V in vitro and in vivo and observations on its effects in experimental animals. Infect Immun 17: 497-503.
24. Seidman CE, Struhl K, Sheen J, Jessen T (2001) Introduction of plasmid DNA into cells. Curr Protoc Mol Biol 1: 1-10.
25. Kado CI, Liu ST (1981) Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145: 1365-1373.
26. Fredericq P (1964) Colicins And Colicinogeny. Ann Inst Pasteur (Paris) 107 (7): 7-17.
27. Touchman JW, Dehejia A, Chiba-Falek O, Cabin DE, Schwartz JR, et al. (2001) Human and mouse alpha-synuclein genes: comparative genomic sequence analysis and identification of a novel gene regulatory element. Genome Res 11: 78-86.
28. Stothard P, Wishart DS (2005) Circular genome visualization and exploration using CGView. Bioinformatics 21: 537-539.
29. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
30. Zahrl D, Wagner M, Bischof K, Koraimann G (2006) Expression and assembly of a functional type IV secretion system elicit extracytoplasmic and cytoplasmic stress responses in Escherichia coli. J Bacteriol 188: 6611-6621.
31. Frost LS, Ippen-Ihler K, Skurray RA (1994) Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol Rev 58: 162-210.
32. Lu J, Manchak J, Klimke W, Davidson C, Firth N, et al. (2002) Analysis and characterization of the IncFV plasmid pED208 transfer region. Plasmid 48: 24-37.
33. Kaniga K, Compton MS, Curtiss III R, Sundaram P (1998) Molecular and functional characterization of Salmonella enterica serovar typhimurium poxA gene: effect on attenuation of virulence and protection. Infect Immun 66: 5599-5606.
34. Lane D, Gardner RC (1979) Second EcoRI fragment of F capable of self-replication. J Bacteriol 139: 141-151.
35. Saadi S, Maas WK, Bergquist PL (1984) RepFIC, a basic replicon of IncFI plasmids that has homology with a basic replicon of IncFII plasmids. Plasmid 12: 61-64.
36. Hiraga S (1992) Chromosome and plasmid partition in Escherichia coli. Annu Rev Biochem 61: 283-306.
37. Lawley TD, Taylor DE (2003) Characterization of the double-partitioning modules of R27: correlating plasmid stability with plasmid localization. J Bacteriol 185: 3060-3067.
38. Gerdes K, Nielsen A, Thorsted P, Wagner EG (1992) Mechanism of killer gene activation. Antisense RNA-dependent RNase III cleavage ensures rapid turnover of the stable hok, srnB and pndA effector messenger RNAs. J Mol Biol 226: 637-649.
39. Hayes F (2003) Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301: 1496-1499.
40. Hollenstein K, Dawson RJ, Locher KP (2007) Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17: 412-418.
41. Davidson AL, Chen J (2004) ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73: 241-268.
42. Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237.
43. Sabri M, Leveille S, Dozois CM (2006) A SitABCD homologue from an avian pathogenic Escherichia coli strain mediates transport of iron and manganese and resistance to hydrogen peroxide. Microbiology 152: 745-758.
44. Crosa JH, Mey AR, Payne SM (2004) Iron transport in bacteria. Washington, D. C.: ASM Press. 499 p.
45. Bearden SW, Perry RD (1999) The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32: 403-414.
46. Lucchini S, Liu H, Jin Q, Hinton JC, Yu J (2005) Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect Immun 73: 88-102.
47. Sabri M, Caza M, Proulx J, Lymberopoulos MH, Bree A, et al. (2008) Contribution of the SitABCD, MntH, and FeoB metal transporters to the virulence of avian pathogenic Escherichia coli O78 strain chi7122. Infect Immun 76: 601-611.
48. Zaharik ML, Cullen VL, Fung AM, Libby SJ, Kujat Choy SL, et al. (2004) The Salmonella enterica serovar typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid model. Infect Immun 72: 5522-5525.
49. Baumler AJ, Norris TL, Lasco T, Voight W, Reissbrodt R, et al. (1998) IroN, a novel outer membrane siderophore receptor characteristic of Salmonella enterica. J Bacteriol 180: 1446-1453.
50. Baumler AJ, Tsolis RM, van der Velden AW, Stojiljkovic I, Anic S, et al. (1996) Identification of a new iron regulated locus of Salmonella typhi. Gene 183: 207-213.
51. Dobrindt U, Blum-Oehler G, Hartsch T, Gottschalk G, Ron EZ, et al. (2001) S-Fimbria-encoding determinant sfa(I) is located on pathogenicity island III(536) of uropathogenic Escherichia coli strain 536. Infect Immun 69: 4248-4256.
52. Hantke K, Nicholson G, Rabsch W, Winkelmann G (2003) Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci U S A 100: 3677-3682.
53. Warner PJ, Williams PH, Bindereif A, Neilands JB (1981) ColV plasmid-specific aerobactin synthesis by invasive strains of Escherichia coli. Infect Immun 33: 540-545.
54. Williams PH, Warner PJ (1980) ColV plasmid-mediated, colicin V-independent iron uptake system of invasive strains of Escherichia coli. Infect Immun 29: 411-416.
55. Crosa JH (1989) Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev 53: 517-530.
56. Valdebenito M, Crumbliss AL, Winkelmann G, Hantke K (2006) Environmental factors influence the production of enterobactin, salmochelin, aerobactin, and yersiniabactin in Escherichia coli strain Nissle 1917. Int J Med Microbiol 296: 513-520.
57. Gilson L, Mahanty HK, Kolter R (1990) Genetic analysis of an MDR-like export system: the secretion of colicin V. Embo J 9: 3875-3884.
58. Gratia A (1925) Sur un remarquable exemple d'antagonisme entre deux souches de colibacille. C R Soc Biol 93: 1040-1042.
59. Zhang LH, Fath MJ, Mahanty HK, Tai PC, Kolter R (1995) Genetic analysis of the colicin V secretion pathway. Genetics 141: 25-32.
60. Wooley RE, Brown J, Gibbs PS, Nolan LK, Turner KR (1994) Effect of normal intestinal flora of chickens on colonization by virulent colicin V-producing, avirulent, and mutant colicin V-producing avian Escherichia coli. Avian Dis 38: 141-145.
61. Quackenbush RL, Falkow S (1979) Relationship between colicin V activity and virulence in Escherichia coli. Infect Immun 24: 562-564.
62. Kobayashi N, Nishino K, Yamaguchi A (2001) Novel macrolide-specific ABC-type efflux transporter in Escherichia coli. J Bacteriol 183: 5639-5644.
63. Provence DL, Curtiss III R (1994) Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect Immun 62: 1369-1380.
64. Maurer JJ, Brown TP, Steffens WL, Thayer SG (1998) The occurrence of ambient temperature-regulated adhesins, curli, and the temperature-sensitive hemagglutinin tsh among avian Escherichia coli. Avian Dis 42: 106-118.
65. Heimer SR, Rasko DA, Lockatell CV, Johnson DE, Mobley HL (2004) Autotransporter genes pic and tsh are associated with Escherichia coli strains that cause acute pyelonephritis and are expressed during urinary tract infection. Infect Immun 72: 593-597.
66. Dutta PR, Cappello R, Navarro-Garcia F, Nataro JP (2002) Functional comparison of serine protease autotransporters of enterobacteriaceae. Infect Immun 70: 7105-7113.
67. Dutta PR, Sui BQ, Nataro JP (2003) Structure-function analysis of the enteroaggregative Escherichia coli plasmid-encoded toxin autotransporter using scanning linker mutagenesis. J Biol Chem 278: 39912-39920.
68. Restieri C, Garriss G, Locas MC, Dozois CM (2007) Autotransporter-encoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl Environ Microbiol 73: 1553-1562.
69. Kostakioti M, Stathopoulos C (2004) Functional analysis of the Tsh autotransporter from an avian pathogenic Escherichia coli strain. Infect Immun 72: 5548-5554.
70. Otto BR, van Dooren SJ, Dozois CM, Luirink J, Oudega B (2002) Escherichia coli hemoglobin protease autotransporter contributes to synergistic abscess formation and heme-dependent growth of Bacteroides fragilis. Infect Immun 70: 5-10.
71. Zienkiewicz M, Kern-Zdanowicz I, Golebiewski M, Zylinska J, Mieczkowski P, et al. (2007) Mosaic structure of p1658/97, a 125-kilobase plasmid harboring an active amplicon with the extended-spectrum beta-lactamase gene blaSHV-5. Antimicrob Agents Chemother 51: 1164-1171.
72. Morales C, Lee MD, Hofacre C, Maurer JJ (2004) Detection of a novel virulence gene and a Salmonella virulence homologue among Escherichia coli isolated from broiler chickens. Foodborne Pathog Dis 1: 160-165.
73. Sugimura K, Nishihara T (1988) Purification, characterization, and primary structure of Escherichia coli protease VII with specificity for paired basic residues: identity of protease VII and OmpT. J Bacteriol 170: 5625-5632.
74. Stathopoulos C (1998) Structural features, physiological roles, and biotechnological applications of the membrane proteases of the OmpT bacterial endopeptidase family: a micro-review. Membr Cell Biol 12: 1-8.
75. Stumpe S, Schmid R, Stephens DL, Georgiou G, Bakker EP (1998) Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of Escherichia coli. J Bacteriol 180: 4002-4006.
76. Cavard D, Lazdunski C (1990) Colicin cleavage by OmpT protease during both entry into and release from Escherichia coli cells. J Bacteriol 172: 648-652.
77. Lundrigan MD, Webb RM (1992) Prevalence of ompT among Escherichia coli isolates of human origin. FEMS Microbiol Lett 76: 51-56.
78. Sodeinde OA, Subrahmanyam YV, Stark K, Quan T, Bao Y, et al. (1992) A surface protease and the invasive character of plague. Science 258: 1004-1007.
79. Burrus V, Waldor MK (2004) Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 155: 376-386.
80. Schneider D, Lenski RE (2004) Dynamics of insertion sequence elements during experimental evolution of bacteria. Res Microbiol 155: 319-327.
81. Johnson JR, Russo TA (2002) Extraintestinal pathogenic Escherichia coli: "the other bad E coli". J Lab Clin Med 139: 155-162.
82. Otto BR, van Dooren SJ, Nuijens JH, Luirink J, Oudega B (1998) Characterization of a hemoglobin protease secreted by the pathogenic Escherichia coli strain EB1. J Exp Med 188: 1091-1103.
83. Mainil JG, Bex F, Dreze P, Kaeckenbeeck A, Couturier M (1992) Replicon typing of virulence plasmids of enterotoxigenic Escherichia coli isolates from cattle. Infect Immun 60: 3376-3380.
84. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, et al. (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21: 3422-3423.